Experimental Hematology
Volume 33, Issue 9 , Pages 1048-1054 , September 2005

Placenta as a site for hematopoietic stem cell development

  • Hanna K.A. Mikkola

      Affiliations

    • Department of Pediatric Oncology, Dana-Farber Cancer Institute and Children's Hospital, Boston, Mass., USA
    • Corresponding Author InformationOffprint requests to: Hanna Mikkola, M.D., Ph.D., Department of Pediatric Oncology, Dana-Farber Cancer Institute, 44 Binney Street, Boston, MA 02115
    • ,
  • Christos Gekas

      Affiliations

    • Department of Pediatric Oncology, Dana-Farber Cancer Institute and Children's Hospital, Boston, Mass., USA
    • ,
  • Stuart H. Orkin

      Affiliations

    • Department of Pediatric Oncology, Dana-Farber Cancer Institute and Children's Hospital, Boston, Mass., USA
    • ,
  • Francoise Dieterlen-Lievre

      Affiliations

    • Laboratorie d'Embryologie cellulaire et moleculaire du CNRS et du College de France, Nogent-s/Marne, France

References 

  1. Turpen JB, Knudson CM, Hoefen PS. The early ontogeny of hematopoietic cells studied by grafting cytogenetically labeled tissue anlagen: localization of a prospective stem cell compartment. Dev Biol. 1981;85:99–112
  2. Dieterlen-Lievre F. On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J Embryol Exp Morphol. 1975;33:607–619
  3. Dieterlen-Lievre F, Martin C. Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev Biol. 1981;88:180–191
  4. Cumano A, Dieterlen-Lievre F, Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell. 1996;86:907–916
  5. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 1996;86:897–906
  6. Peault B, Tavian M, Matsuoka S, et al. Hematopoietic stem cell emergence in the human embryo and fetus. Ann N Y Acad Sci. 2003;996:132–140
  7. Kumaravelu P, Hook L, Morrison AM, et al. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development. 2002;129:4891–4899
  8. Till JE, McCulloch EA. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961;14:212–222
  9. Dancis J, Jansen V, Gorstein F, Douglas GW. Hematopoietic cells in mouse placenta. Am J Obstet Gynecol. 1968;100:1110–1121
  10. Dancis J, Jansen V, Brown GF, Gorstein F, Balis ME. Treatment of hypoplastic anemia in mice with placental transplants. Blood. 1977;50:663–670
  11. Melchers F. Murine embryonic B lymphocyte development in the placenta. Nature. 1979;277:219–221
  12. Caprioli A, Jaffredo T, Gautier R, Dubourg C, Dieterlen-Lievre F. Blood-borne seeding by hematopoietic and endothelial precursors from the allantois. Proc Natl Acad Sci U S A. 1998;95:1641–1646
  13. Caprioli A, Minko K, Drevon C, et al. Hemangioblast commitment in the avian allantois: cellular and molecular aspects. Dev Biol. 2001;238:64–78
  14. Alvarez-Silva M, Belo-Diabangouaya P, Salaun J, Dieterlen-Lievre F. Mouse placenta is a major hematopoietic organ. Development. 2003;130:5437–5444
  15. Gekas C, Dieterlen-Lievre F, Orkin SH, Mikkola HK. The placenta is a niche for hematopoietic stem cells. Dev Cell. 2005;8:365–375
  16. Ottersbach K, Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell. 2005;8:377–387
  17. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet. 2001;2:538–548
  18. Cross JC, Baczyk D, Dobric N, et al. Genes, development and evolution of the placenta. Placenta. 2003;24:123–130
  19. Downs KM. Early placental ontogeny in the mouse. Placenta. 2002;23:116–131
  20. Downs KM, Gardner RL. An investigation into early placental ontogeny: allantoic attachment to the chorion is selective and developmentally regulated. Development. 1995;121:407–416
  21. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science. 1998;282:2072–2075
  22. Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development. 1999;126:5073–5084
  23. Cumano A, Ferraz JC, Klaine M, Di Santo JP, Godin I. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity. 2001;15:477–485
  24. Yoder MC, Hiatt K, Mukherjee P. In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A. 1997;94:6776–6780
  25. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242–245
  26. Sanchez MJ, Holmes A, Miles C, Dzierzak E. Characterization of the first definitive hematopoietic stem cells in the AGM and liver of the mouse embryo. Immunity. 1996;5:513–525
  27. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 1997;7:335–344
  28. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ, Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity. 2002;16:673–683
  29. Ma X, Robin C, Ottersbach K, Dzierzak E. The Ly-6A (Sca-1) GFP transgene is expressed in all adult mouse hematopoietic stem cells. Stem Cells. 2002;20:514–521
  30. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood. 2003;101:508–516
  31. Ferkowicz MJ, Starr M, Xie X, et al. CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development. 2003;130:4393–4403
  32. Corbel C, Salaun J. αIIb integrin expression during development of the murine hemopoietic system. Dev Biol. 2002;243:301–311
  33. Bertrand JY, Giroux S, Golub R, et al. Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc Natl Acad Sci U S A. 2005;102:134–139
  34. Palis J, Yoder MC. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol. 2001;29:927–936
  35. Dieterlen-Lièvre F. Intraembryonic hematopoietic stem cells. In:  Zon LI editors. Hematology/Oncology Clinics of North America 11. Philadelphia: WB Saunders Company; 1997;p. 1149–1171
  36. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432:625–630
  37. Douagi I, Vieira P, Cumano A. Lymphocyte commitment during embryonic development, in the mouse. Semin Immunol. 2002;14:361–369
  38. Houssaint E. Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Differ. 1981;10:243–252
  39. McGrath KE, Koniski AD, Malik J, et al. Circulation is established in a stepwise pattern in the mammalian embryo. Blood. 2003;101:1669–1676
  40. Christensen JL, Wright DE, Wagers AJ, Weissman IL. Circulation and chemotaxis of fetal hematopoietic stem cells. PLoS Biol. 2004;2:E75
  41. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841–846
  42. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836–841

PII: S0301-472X(05)00293-6

doi: 10.1016/j.exphem.2005.06.011

Experimental Hematology
Volume 33, Issue 9 , Pages 1048-1054 , September 2005

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